Maternal effect and speciation: maternal effect contributes to the evolution of hybrid inviability between Drosophila simulans and Drosophila mauritiana

Genome ◽  
2015 ◽  
Vol 58 (9) ◽  
pp. 405-413
Author(s):  
Sogol Eizadshenass ◽  
Rama S. Singh
Keyword(s):  
Maternal Effects ◽  
Maternal Effect ◽  
Genetic Basis ◽  
Drosophila Simulans ◽  
Hybrid Male ◽  
Egg Hatching ◽  
Hybrid Inviability ◽  
F1 Hybrid ◽  
Drosophila Mauritiana ◽  
Negative Effect

Haldane’s rule has been the basis of speciation research during the last 30 years. Most studies have focused on the nature of incompatibilities in the hybrid male, but not much attention has been given to the genetic basis of fertility and inviability in hybrid females. Hybridizations between Drosophila simulans and Drosophila mauritiana produce fertile females and sterile males. Here, we re-examined the level of fertility in reciprocal F1 females of these two species and looked for the presence of maternal effects. Our results show that the reciprocal F1 females of D. simulans and D. mauritiana hybridizations are fully fertile and in fact show a significant level of heterosis in the rate of oviposition but display reduced egg hatching in one direction. Reduced egg hatching was observed in the progenies of F1 hybrid females with D. mauritiana as mother, the same cross that showed a stronger negative effect on F1 male fertility. A review of the literature on the hybridizations in Lepidoptera also showed a maternal effect on inviability when reciprocal crosses produced asymmetric results. Our findings point to the importance of maternal effects in the evolution of embryo inviability and thus enhancing the process of speciation through the evolution of hybrid inviability.

scholarly journals The genetic basis of Haldane's rule and the nature of asymmetric hybrid male sterility among Drosophila simulans, Drosophila mauritiana and Drosophila sechellia.

Genetics ◽  
1993 ◽  
Vol 134 (1) ◽  
pp. 251-260 ◽  
Author(s):  
L W Zeng ◽  
R S Singh
Keyword(s):  
Male Sterility ◽  
Y Chromosome ◽  
Genetic Basis ◽  
Drosophila Simulans ◽  
Hybrid Male ◽  
Hybrid Male Sterility ◽  
Haldane’S Rule ◽  
Drosophila Sechellia ◽  
Haldane's Rule ◽  
Drosophila Mauritiana

Abstract Haldane's rule (i.e., the preferential hybrid sterility and inviability of heterogametic sex) has been known for 70 years, but its genetic basis, which is crucial to the understanding of the process of species formation, remains unclear. In the present study, we have investigated the genetic basis of hybrid male sterility using Drosophila simulans, Drosophila mauritiana and Drosophila sechellia. An introgression of D. sechellia Y chromosome into a fairly homogenous background of D. simulans did not show any effect of the introgressed Y on male sterility. The substitution of D. simulans Y chromosome into D. sechellia, and both reciprocal Y chromosome substitutions between D. simulans and D. mauritiana were unsuccessful. Introgressions of cytoplasm between D. simulans and D. mauritiana (or D. sechellia) also did not have any effect on hybrid male sterility. These results rule out the X-Y interaction hypothesis as a general explanation of Haldane's rule in this species group and indicate an involvement of an X-autosome interaction. Models of symmetrical and asymmetrical X-autosome interaction have been developed which explain the Y chromosome substitution results and suggest that evolution of interactions between different genetic elements in the early stages of speciation is more likely to be of an asymmetrical nature. The model of asymmetrical X-autosome interaction also predicts that different sets of interacting genes may be involved in different pairs of related species and can account for the observation that hybrid male sterility in many partially isolated species is often nonreciprocal or unidirectional.

Evidence for complex genic interactions between conspecific chromosomes underlying hybrid female sterility in the Drosophila simulans clade.

Genetics ◽  
1994 ◽  
Vol 137 (1) ◽  
pp. 191-199 ◽  
Author(s):  
A W Davis ◽  
E G Noonburg ◽  
C I Wu
Keyword(s):  
Hybrid Sterility ◽  
Drosophila Simulans ◽  
Female Sterility ◽  
Hybrid Male ◽  
Hybrid Female ◽  
Hybrid Male Sterility ◽  
Epistatic Interactions ◽  
X Chromosomes ◽  
F1 Hybrid ◽  
Drosophila Mauritiana

Abstract F1 hybrid females between the sibling species Drosophila simulans, Drosophila mauritiana and Drosophila sechellia are completely fertile. However, we have found that female sterility can be observed in F2 backcross females who are homozygous for D. simulans X chromosomes and homozygous for autosomal regions from either D. mauritiana or D. sechellia. Our results indicate that neither D. mauritiana autosome (2 or 3) can cause complete female sterility in a D. simulans background. The simultaneous presence of homozygous regions from both the second and third chromosomes of D. mauritiana, however, causes nearly complete female sterility which cannot be accounted for by their individual effects. The two autosomes of D. sechellia may show a similar pattern. From the same crosses, we also obtained evidence against a role for cytoplasmic or maternal effects in causing hybrid male sterility between these species. Taken with the results presented elsewhere, these observations suggest that epistatic interactions between conspecific genes in a hybrid background may be the prevalent mode of hybrid sterility between recently diverged species.

A Novel System of Fertility Rescue in Drosophila Hybrids Reveals a Link Between Hybrid Lethality and Female Sterility

Genetics ◽  
2003 ◽  
Vol 163 (1) ◽  
pp. 217-226 ◽  
Author(s):  
Daniel A Barbash ◽  
Michael Ashburner
Keyword(s):  
Drosophila Melanogaster ◽  
Low Temperature ◽  
Genetic Basis ◽  
Female Sterility ◽  
Hybrid Lethality ◽  
Hybrid Male ◽  
Hybrid Female ◽  
F1 Hybrid ◽  
Drosophila Gene

Abstract Hybrid daughters of crosses between Drosophila melanogaster females and males from the D. simulans species clade are fully viable at low temperature but have agametic ovaries and are thus sterile. We report here that mutations in the D. melanogaster gene Hybrid male rescue (Hmr), along with unidentified polymorphic factors, rescue this agametic phenotype in both D. melanogaster/D. simulans and D. melanogaster/D. mauritiana F1 female hybrids. These hybrids produced small numbers of progeny in backcrosses, their low fecundity being caused by incomplete rescue of oogenesis as well as by zygotic lethality. F1 hybrid males from these crosses remained fully sterile. Hmr+ is the first Drosophila gene shown to cause hybrid female sterility. These results also suggest that, while there is some common genetic basis to hybrid lethality and female sterility in D. melanogaster, hybrid females are more sensitive to fertility defects than to lethality.

scholarly journals Genetic basis to hybrid inviability is more complex than hybrid male sterility in Caenorhabditis nematodes

Heredity ◽  
2018 ◽  
Vol 121 (2) ◽  
pp. 169-182 ◽  
Author(s):  
Joanna D. Bundus ◽  
Donglin Wang ◽  
Asher D. Cutter
Keyword(s):  
Male Sterility ◽  
Genetic Basis ◽  
Hybrid Male ◽  
Hybrid Male Sterility ◽  
Hybrid Inviability

Genetics of reproductive isolation in the Drosophila simulans clade: complex epistasis underlying hybrid male sterility.

Genetics ◽  
1994 ◽  
Vol 137 (1) ◽  
pp. 175-189 ◽  
Author(s):  
E L Cabot ◽  
A W Davis ◽  
N A Johnson ◽  
C I Wu
Keyword(s):  
Male Sterility ◽  
Genetic Basis ◽  
Species Differences ◽  
Single Gene ◽  
Hybrid Sterility ◽  
Drosophila Simulans ◽  
Theoretical Argument ◽  
Hybrid Male ◽  
Individual Factor ◽  
Resolution Mapping

Abstract We have analyzed the sterility associated with introgressions of the distal one-fourth of the X chromosome from either Drosophila mauritiana or Drosophila sechellia into the genome of Drosophila simulans using a series of visible and DNA markers. Because in Drosophila hybrids, male sterility is usually complete and is often tightly linked with each of several markers used in crosses, a simple genetic basis has generally been assumed. In our low resolution mapping experiment, we were not able to reject the null hypothesis that a single gene, introgressed from either D. mauritiana or D. sechellia, is the cause of male sterility. High resolution mapping, however, reveals a much more complex picture. At least three distinct factors from D. mauritiana, or two from D. sechellia, were identified that need to be jointly present to confer full sterility. Each individual factor by itself is relatively ineffective in causing sterility, or even a partial spermatogenic defect. Moreover, there appear to be more sterility factors on comparable introgressions from D. mauritiana than from D. sechellia. On the basis of these observations, we propose a model which suggests that multilocus weak allele interactions are a very common cause of reproductive incompatibility between closely related species. We also present theoretical argument and empirical evidence against extrapolating the results of within-species analysis to interpret the genetic basis of species differences. The implications of this model on the theories of evolution of species differences and the attempt to understand the mechanisms of hybrid sterility/inviability at the molecular level are discussed.

scholarly journals The Genetics of Reproductive Isolation in the Drosophila simulans Clade: X vs. Autosomal Effects and Male vs. Female Effects

Genetics ◽  
1996 ◽  
Vol 143 (3) ◽  
pp. 1243-1255 ◽  
Author(s):  
Hope Hollocher ◽  
Chug-I Wu
Keyword(s):  
Reproductive Isolation ◽  
Male Sterility ◽  
X Chromosome ◽  
Hybrid Sterility ◽  
Drosophila Simulans ◽  
Female Sterility ◽  
Hybrid Male ◽  
Hybrid Female ◽  
Hybrid Male Sterility ◽  
Hybrid Inviability

Abstract A strong effect of homozygous autosomal regions on reproductive isolation was found for crosses between the species in the Drosophila simulans clade. Second chromosome regions were introgressed from D. mauritiana and D. sechellia into D. simulans and tested for their homozygous effects on hybrid male and hybrid female sterility and inviability. Most introgressions are fertile as heterozygotes, yet produce sterile male offspring when made homozygous. The density of homozygous autosomal factors contributing to hybrid male sterility is comparable to the density of X chromosome factors for this level of resolution. Female sterility was also revealed, yet the disparity between male and female levels of sterility was great, with male sterility being up to 23 times greater than female sterility. Complete hybrid inviability was also associated with some regions of the second chromosome, yet there were no strong sex differences. In conclusion, we find no evidence to support a strong X chromosome bias in the evolution of hybrid sterility or inviability but do find a very strong sex bias in the evolution of hybrid sterility. In light of these findings, we reevaluate the current models proposed to explain the genetic pattern of reproductive isolation.

scholarly journals Genetics of reproductive isolation in the Drosophila simulans clade: DNA marker-assisted mapping and characterization of a hybrid-male sterility gene, Odysseus (Ods).

Genetics ◽  
1993 ◽  
Vol 134 (1) ◽  
pp. 261-275 ◽  
Author(s):  
D E Perez ◽  
C I Wu ◽  
N A Johnson ◽  
M L Wu
Keyword(s):  
Male Sterility ◽  
Major Gene ◽  
Drosophila Simulans ◽  
Recombination Analysis ◽  
Hybrid Male ◽  
Hybrid Male Sterility ◽  
Complete Penetrance ◽  
Drosophila Mauritiana ◽  
Male Sterility Gene

Abstract In this study, we address the question of whether there exist major genes that cause complete male sterility in the interspecific hybrids of Drosophila and, if they do, how these genes may be characterized at the molecular level. Our approach is to introgress small segments of the X chromosome from Drosophila mauritiana (or Drosophila sechellia) into Drosophila simulans by repeated backcrosses for more than 20 generations. The introgressions are monitored by both visible mutations and a series of DNA markers. We compare the extent of introgressions that cause male sterility with those that do not. If a major sterility factor exists, there should be a sharp boundary between these two classes of introgressions and their breakpoints should demarcate such a gene. Furthermore, if male sterility is the only major fitness effect associated with the introgression, recombination analysis should yield a pattern predicted by the classical three-point cross. Both the genetic and molecular analyses suggest the presence of a major sterility factor from D. mauritiana, which we named Odysseus (Ods), in the cytological interval of 16D. We thus formalize three criteria for inferring the existence of a major gene within an introgression: (1) complete penetrance of sterility, (2) complementarity in recombination analysis, and (3) physical demarcation. Introgressions of Ods from D. sechellia do not cause sterility. Twenty-two introgressions in our collection have breakpoints in this interval of about 500 kb, making it possible to delineate Ods more precisely for molecular identification. The recombination analysis also reveals the complexity of the introgressed segments--even relatively short ones may contain a second male sterility factor and partial viability genes and may also interfere with crossovers. The spermatogenic defects associated with Ods and/or a second factor were characterized by phase-contrast microscopy.

scholarly journals Epistatic Control of Non-Mendelian Inheritance in Mouse Interspecific Crosses

Genetics ◽  
1996 ◽  
Vol 143 (4) ◽  
pp. 1739-1752 ◽  
Author(s):  
Xavier Montagutelli ◽  
Rowena Turner ◽  
Joseph H Nadeau
Keyword(s):  
X Chromosome ◽  
Genetic Basis ◽  
Mendelian Inheritance ◽  
The Other ◽  
Interspecific Crosses ◽  
Chromosome 2 ◽  
Mus Spretus ◽  
F1 Hybrid ◽  
Strong Deviation ◽  
Marker Loci

Abstract Strong deviation of allele frequencies from Mendelian inheritance favoring Mus spretus-derived alleles has been described previously for X-linked loci in four mouse interspecific crosses. We reanalyzed data for three of these crosses focusing on the location of the gene(s) controlling deviation on the X chromosome and the genetic basis for incomplete deviation. At least two loci control deviation on the X chromosome, one near Xist (the candidate gene controlling X inactivation) and the other more centromerically located. In all three crosses, strong epistasis was found between loci near Xist and marker loci on the central portion of chromosome 2. The mechanism for this deviation from Mendelian expectations is not yet known but it is probably based on lethality of embryos carrying particular combinations of alleles rather than true segregation distortion during oogenesis in F1 hybrid females.

scholarly journals Hidden Effects of X Chromosome Introgressions on Spermatogenesis in Drosophila simulans × D. mauritiana Hybrids Unveiled by Interactions Among Minor Genetic Factors

Genetics ◽  
1998 ◽  
Vol 150 (2) ◽  
pp. 745-754 ◽  
Author(s):  
Xulio R Maside ◽  
José P Barral ◽  
Horacio F Naveira
Keyword(s):  
Male Sterility ◽  
X Chromosome ◽  
Seminal Vesicles ◽  
Genetic Dissection ◽  
Research Strategies ◽  
Hybrid Male ◽  
Hybrid Male Sterility ◽  
Epistatic Interactions ◽  
Drosophila Mauritiana ◽  
Chromosome Segments

Abstract One of the most frequent outcomes of interspecific hybridizations in Drosophila is hybrid male sterility. Genetic dissection of this reproductive barrier has revealed that the number of responsible factors is very high and that these factors are frequently engaged in complex epistatic interactions. Traditionally, research strategies have been based on contrasting introgressions of chromosome segments that produce male sterility with those that allow fertility. Few studies have investigated the phenotypes associated with the boundary between fertility and sterility. In this study, we cointrogressed three different X chromosome segments from Drosophila mauritiana into D. simulans. Hybrid males with these three segments are usually fertile, by conventional fertility assays. However, their spermatogenesis shows a significant slowdown, most manifest at lower temperatures. Each of the three introgressed segments retards the arrival of sperm to the seminal vesicles. Other small disturbances in spermatogenesis are evident, which altogether lead to an overall reduction in the amount of motile sperm in their seminal vesicles. These results suggest that a delay in the timing of spermatogenesis, which might be brought about by the cumulative action of many different factors of minor segment, may be the primary cause of hybrid male sterility.

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